The document summarizes research conducted by Timothy Mousseau and Anders Møller on the impacts of radiation exposure from Chernobyl on natural populations. Their Chernobyl Research Initiative has studied birds, insects, microbes and plants near Chernobyl since 2000. It lists 48 scientific publications produced by the initiative investigating topics like mutation rates, population declines, sperm quality, DNA damage and more. The research aims to document adaptation and the impacts of elevated mutation rates on populations.
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Myth: Chernobyl's eco-system is thriving
1. Chernobyl, Fukushima, and Other Hot Places
Timothy A. Mousseau1 & Anders P. Møller2
Andrea Bonisoli-Alquati1
Gennadi Milinevski3
1 University of South Carolina
2 CNRS, France
3 Taras Shevchenko University of Kyiv
Sponsored by:
The Samuel Freeman Charitable Trust,
USC College of Arts & Sciences,
USC Office of Research, CNRS (France),
Fulbright Foundation, Qiagen GmbH, National Science Foundation,
National Institutes of Health, National Geographic Society, CRDF, NATO
2. Chernobyl Research Initiative
• Began in 2000 by T.A. Mousseau and A.P. Møller
• Studies of natural populations of birds, insects, microbes
and plants.
• Studies of the Children of the Narodichesky region of
Ukraine.
• As evolutionary biologists, mainly interested in documenting
adaptation and impacts of elevated mutation rates on
population processes.
3. Scientific Publications by the Chernobyl Research Initiative (Moller, Mousseau, et al.) since 2001:
http://cricket.biol.sc.edu/chernobyl/
1. Møller, A.P., I. Nishiumi, H. Suzuki, K. Ueda, and T.A. Mousseau. 2013. Differences in effects of radiation on abundance of
animals in Fukushima and Chernobyl. Ecological Indicators, in press.
2. Mousseau, T.A., Møller, A.P. 2012. Chernobyl and Fukushima: Differences and Similarities, a biological perspective.
Asian Perspective, in press.
3. Svendsen, E.R., J.R. Runkle, V.R. Dhara, S. Lin, M. Naboka, T. Mousseau, C. Bennett. 2012. Epidemiological lessons learned
from environmental public health disasters: Chernobyl, the World Trade Center, Bhopal, and Graniteville, South Carolina.
International Journal of Environmental Research and Public Health, 9 (doi:10.3390/ijerph90x00x), in press.
4. Møller, A.P. and T.A. Mousseau. 2012. The effects of natural variation in background radioactivity on humans, animals
and other organisms. Biological Reviews, in press.
5. Møller, A.P., F. Barnier, and T.A. Mousseau. 2012. Ecosystem effects 25 years after Chernobyl: pollinators, fruit set, and
recruitment. Oecologia, in press.
6. Beasley, D.A.E., A. Bonisoli-Alquati, S.M. Welch, A. P. Møller, T.A. Mousseau. Effects of parental radiation exposure on
developmental instability in grasshoppers (Chorthippus albomarginatus). Journal of Evolutionary Biology, in press.
7. Møller, A.P., A. Hagiwara, S. Matsui, S. Kasahara, K. Kawatsu, I. Nishiumi, H. Suzuki, K. Ueda, and T.A. Mousseau. 2012.
Abundance of birds in Fukushima as judged from Chernobyl. Environmental Pollution, 164:36-39.
8. Møller, A.P., A. Bonisoli-Alquati, G. Rudolfsen, T.A. Mousseau. Elevated mortality among birds in Chernobyl as judged
from biased sex and age ratios. PLoS One, 7(4):e35223.
9. Møller, A. P., and T.A. Mousseau. 2011. Conservation consequences of Chernobyl and other nuclear accidents. Biological
Conservation, 144:2787-2798.
10. Mousseau, T.A. and A.P. Møller. 2011. Landscape portrait: A look at the impacts of radioactive contaminants on
Chernobyl’s wildlife. Bulletin of the Atomic Scientists. 67(2): 38-46. (DOI: 10.1177/0096340211399747)
11. Redchuk, T.A., A.I. Rozhok, O.W. Zhuk, I. A. Kozeretska, and T.A. Mousseau. 2012. DNA Methylation in Drosophila
melanogaster may depend on lineage heterogeneity. Cytology and Genetics, ISSN 0095-4527; 46:58-61.
12. Galvan, I., T.A. Mousseau, and A.P. Møller. 2011. Bird population declines due to radiation exposure at Chernobyl are
stronger in species with pheomelanin-based coloration. Oecologia 165(4): 827-835 (DOI 10.1007/s00422-010-1860-5)
13. Balbontín, J., F. de Lope, I. G. Hermosell, T. A. Mousseau and A. P. Møller. 2011. Determinants of age-dependent change
in a secondary sexual character. Journal of Evolutionary Biology 24(2): 440-448. DOI: 10.1111/j.1420-9101.2010.02183.x
14. Møller, A.P. and T.A. Mousseau. 2011. Ten ecological and evolutionary questions about Chernobyl. Bulletin of the
Chernobyl Zone. In press.
15. Bonisoli-Alquati, A., A.P. Møller., G. Rudolfsen, N. Saino, M. Caprioli, S. Ostermiller, T.A. Mousseau. 2011. The effects of
radiation on sperm swimming behavior depend on plasma oxidative status in the barn swallow (Hirundo rustica).
Comparative Biochemistry and Physiology – Part A – Molecular & Integrative Physiology, 159(2): 105-112. DOI:
10.1016/j.cbpa.2011.01.018
16. Møller, A. P., & T.A. Mousseau. 2011. Efficiency of bio-indicators for low-level radiation under field conditions. Ecological
Indicators, 11 (2): 424-430. DOI: 10.1016.j.ecolind.2010.06.013
17. Møller, A.P., A. Bonisoli-Alquati, G. Rudolfsen, and T.A. Mousseau. 2011. Chernobyl birds have smaller brains. Public
Library of Science – One, 6(2): Art. No. e16862. DOI: 10.1371/journal.pone.0016862
18. Serga, S.V., A.I. Rozhok, O.V. Protsenko, I.A. Kozeretska, and T.A. Mousseau. 2010. Spiroplasma in natural populations
of Drosophila melanogaster from Ukraine. Drosophila Information Service, 93: 148-154.
19. Møller, A.P., J. Erritzoe, F. Karadas, and T. A. Mousseau. 2010. Historical mutation rates predict susceptibility to radiation
in Chernobyl birds. Journal of Evolutionary Biology, 23(10): 2132-2142. DOI: 10.1111/j.1420-9101.2010.02074.x
20. Bonisoli-Alquati, A., , A. Voris, T. A. Mousseau, A. P. Møller, N. Saino, and M. Wyatt. 2010. DNA damage in barn swallows
(Hirundo rustica) from the Chernobyl region detected by the use of the Comet assay. Comparative Biochemistry and
Physiology C- Toxicology & Pharmacology 151: 271-277.
21. Bonisoli-Alquati, A., T. A. Mousseau, A. P. Møller, M. Caprioli, and N. Saino. 2010. Increased oxidative stress in barn
swallows from the Chernobyl region. Comparative Biochemistry and Physiology. Part A: Molecular & Integrative
Physiology, 155: 205-210.
22. Czirjak, G.A., A.P. Møller, T.A. Mousseau, P. Heeb. 2010. Microorganisms associated with feathers of barn swallows in
radioactively contaminated areas around Chernobyl. Microbial Ecology 60(2): 373-380.
23. E.R. Svendsen, I.E. Kolpakov, Y.I. Stepanova, V.Y. Vdovenko, M.V. Naboka, T.A. Mousseau, L.C. Mohr, D.G. Hoel, W.J.J.
Karmaus. 2010. 137Cesium exposure and spirometry measures in Ukrainian children affected by the Chernobyl nuclear
incident. Environmental Health Perspectives, 118: 720-725 .
24. Møller, A.P., and T.A. Mousseau. 2009. Reduced abundance of insects and spiders linked to radiation at Chernobyl 20
years after the accident. Biology Letters of the Royal Society 5(3): 356-359.
25. Kravets, A.P., Mousseau, T.A., Litvinchuk, A.V., Ostermiller, S. 2010. Association of P-Mobile element activity and DNA
methylation pattern changes in conditions of Drosophila melanogaster prolonged irradiation. Cytology and Genetics
44(4): 217-220.
26. Kravets А.P, T.A. Musse (T.A. Mousseau), Omel’chenko1 Zh. A., Vengjen G.S. 2010. Dynamics of hybrid dysgenesis
frequency in Drosophila melanogaster in controlled terms of protracted radiation exposure. Cytology and Genetics,
44(4): 262.
27. Kravets А.P, T.A. Musse (T.A. Mousseau), Omel’chenko1 Zh. A., Vengjen G.S. 2010. Dynamics of hybrid dysgenesis
frequency in Drosophila melanogaster in controlled terms of protracted radiation exposure. Cytology and Genetics,
44(3): 144-148.
28. Kravets A.P., Mousseau T.A., Litvinchuk A.V., Ostermiller S., Vengzhen G.S. and D.M. Grodzinskiy. 2010. Wheat plant
DNA methylation pattern changes at chronic seed γ- irradiation. Cytology and Genetics, 44(5): 276-279.
29. Kravets A.P., T.A. Mousseau, Omel’chenko1 Zh. A. 2010. Transformation of dose dependences of P-mobile element
activity following acute and chronic radiation. Radiation Biology & Radioecology, in press (in Russian).
30. Gaschak, S., M. Bondarkov, Ju. Makluk, A. Maksimenko, V. Martynenko, I. Chizhevsky, and T.A. Mousseau. 2009.
Assessment of radionuclide export from Chernobyl zone via birds 18 years following the accident. Radioprotection 44(5):
849-852.
31. Stepanova, E., W. Karmaus, M. Naboka, V. Vdovenko, T. Mousseau, V. Shestopalov, J. Vena, E. Svendsen, D. Underhill,
and H. Pastides. 2008. Exposure from the Chernobyl accident had adverse effects on erythrocytes, leukocytes, and,
platelets in children in the Narodichesky region, Ukraine. A 6-year follow-up study. Environmental Health, 7:21.
32. Kozeretska, I.A., A.V. Protsenko, E.S. Afanas’eva, S.R. Rushkovskii, A.I. Chuba, T.A. Mousseau, and A.P. Møller. 2008.
Mutation processes in natural populations of Drosophila melanogaster and Hirundo rustica from radiation-
contaminated regions of Ukraine. Cytology and Genetics 42(4) : 267-271.
33. Møller, A. P., T.A Mousseau. 2008. Reduced abundance of raptors in radioactively contaminated areas near Chernobyl.
Journal of Ornithology, 150(1):239-246.
34. Møller, A. P., T.A. Mousseau and G. Rudolfsen. 2008. Females affect sperm swimming performance : a field experiment
with barn swallows Hirundo rustica. Behavioral Ecology 19(6):1343-1350.
35. Møller, A. P., F. Karadas, & T. A. Mousseau. 2008. Antioxidants in eggs of great tits Parus major from Chernobyl and
hatching success. J. Comp. Physiol. B. 178:735-743.
36. Gashak, S.P., Y.A. Maklyuk, A.M. Maksimenko, V.M. Maksimenko, V.I. Martinenko, I.V. Chizhevsky, M.D. Bondarkov,
T.A. Mousseau. 2008. The features of radioactive contamination of small birds in Chernobyl Zone in 2003-2005.
Radiobiology and Radioecology 48: 27-47.(Russian).
37. Møller, A. P., T. A. Mousseau, C. Lynn, S. Ostermiller, and G. Rudolfsen. 2008. Impaired swimming behavior and
morphology of sperm from barn swallows Hirundo rustica in Chernobyl. Mutation Research, Genetic Toxicology and
Environmental Mutagenesis, 650:210-216.
38. Møller, A. P., T. A. Mousseau, F. de Lope and N. Saino. 2008. Anecdotes and empirical research in Chernobyl. Biology
Letters, 4:65-66.
39. A.P. Møller, T.A Mousseau. 2007. Species richness and abundance of forest birds in relation to radiation at Chernobyl.
Biology Letters of the Royal Society, 3: 483-486.
40. A.P. Møller, T.A Mousseau. 2007. Determinants of interspecific variation in population declines of birds after exposure
to radiation at Chernobyl. Journal of Applied Ecology, 44: 909-919.
41. A.P. Møller, T.A Mousseau . 2007. Birds prefer to breed in sites with low radioactivity in Chernobyl. Proceedings of the
Royal Society, 274:1443-1448.
42. A.P. Møller, T.A. Mousseau, F. de Lope, and N. Saino. 2007. Elevated frequency of abnormalities in barn swallows from
Chernobyl. Biology Letters of the Royal Society, 3: 414-417.
43. O.V. Tsyusko, M.B. Peters, C. Hagen, T.D. Tuberville, T.A. Mousseau, A.P. Møller and T.C. Glenn. 2007. Microsatellite
markers isolated from barn swallows (Hirundo rustica). Molecular Ecology Notes, 7: 833-835.
44. A. P. Møller, T. A. Mousseau. 2006. Biological consequences of Chernobyl: 20 years after the disaster. Trends in
Ecology and Evolution, 21: 200-207.
45. A. P. Møller, K. A. Hobson, T. A. Mousseau and A. M. Peklo. 2006. Chernobyl as a population sink for barn swallows:
Tracking dispersal using stable isotope profiles. Ecological Applications, 16:1696-1705.
46. A. P. Møller, T. A. Mousseau, G. Milinevsky, A. Peklo, E. Pysanets and T. Szép. 2005. Condition, reproduction and survival
of barn swallows from Chernobyl. Journal of Animal Ecology, 74: 1102-1111.
47. Møller, A. P., Surai, P., and T. A. Mousseau. 2004. Antioxidants, radiation and mutations in barn swallows from
Chernobyl. Proceedings of the Royal Society, London, 272: 247-252.
48. Shestopalov, V., M. Naboka, E. Stepanova, E. Skvarska, T. Mousseau, and Y.Serkis. 2004. Risk assessment of morbidity
under conditions with different levels of radionuclides and heavy metals. Bulletin of the Chernobyl Zone 24(2): 40-47.
(In Ukrainian).
49. Møller, A. P., and T. A. Mousseau. 2003. Mutation and sexual selection: A test using barn swallows from Chernobyl.
Evolution, 57: 2139-2146.
50. Møller, A. P. and T. A. Mousseau . 2001. Albinism and phenotype of barn swallows Hirundo rustica from Chernobyl.
Evolution, 55 (10): 2097-2104.
4. Major Findings from studies of Wildlife in Chernobyl and Fukushima:
1) Most organisms studied show significantly increased rates of genetic
damage in direct proportion to the level of exposure to radioactive
contaminants
2) Many organisms show increased rates of deformities and developmental
abnormalities in direct proportion to contamination levels
3) Many organisms show reduced fertility rates…..
4) Many organisms show reduced life spans……
5) Many organisms show reduced population sizes…..
6) Biodiversity is significantly decreased…… many species locally extinct.
7) Mutations are passed from one generation to the next, and show signs
of accumulating over time.
8) Mutations are migrating out of affected areas into populations that are
not exposed (i.e. population bystander effects).
5. The Barn Swallow,
Hirundo rustica
Animal Models – Provide Clues to Human Populations
Birds don’t usually drink, smoke or get depressed!
Phylopatric
6. Hypotheses and questions addressed:
• Do low (and high) doses result in measureable,
elevated mutation rates in natural populations?
• Are there phenotypic consequences to elevated
mutation rates? (i.e. teratology).
• Are there fitness consequences to elevated
mutation rates? (i.e. survival, reproduction, or
disease). Is there evidence for adaptation?
• Are there effects on population abundances and
biodiversity?
• Are there ecosystem consequences?
7. Massively Replicated Biotic Inventories
(700 in Fukushima, 896 in Chernobyl)
+
Measures of Multiple Environmental Variables
(e.g. meteorology, hydrology, geology, plant community, Habitat type,
land use history, plant coverage amount and type, altitude,
meteorological conditions, time, date, distance to nearest water source, etc)
+
Field Measures of Residential Radiation Levels
+
GIS
+
Multivariate Statistics
=
Predictive Models of Radiation Effects on Populations
8. 896 bird and insect
surveys from
locations in Ukraine
and Belarus
Control Populations:
- Italy (Milan)
- Spain (Badajoz)
- Denmark (Aalborg)
- Ukraine (Borispil)
17. Activity vs Environmental Measurements
N = 279; slope = 0.57 (0.03 SE);
t278 = 15.52; P < 0.0001; R2 = 0.47
June
N = 307; slope = 0.63 (0.03 SE);
t306 = 18.66; P < 0.0001; R2 = 0.53
May
18. External Dose Correlates with Radiation at First
Capture
N = 75; slope = 0.016 (0.001 SE);
t74 = 16.42; P < 0.0001; R2 = 0.79
This is where most
Radioecology studies
end….
19. The UN Chernobyl Forum Report
(IAEA, 2006: p137):
“. . . the populations of many plants and animals have
expanded, and the present environmental conditions have
had a positive impact on the biota in the Chernobyl
Exclusion Zone.”
Human morbidities primarily the result of psychological
stress….
But:
No quantitative data in support of this position and it avoids the
primary question of whether or not there are injuries to
populations and the ecosystem as a result of radioactive
contaminants.
20.
21. The return of plants, animals and
people give the appearance that
health and environmental
consequences of radioactive
contaminants are negligible.
Is this correct?
In 2005, no data available to accept
or refute this hypothesis.
Chernobyl in Recovery?
22.
23. Abundance of birds depressed by
more than 66%
Moller & Mousseau. 2007. Biology Letters of the Royal Society
Moller & Mousseau. 2010. Ecological Indicators.
Micro Sv / hr .
24. Moller & Mousseau. 2007. J. Applied Ecology
Long distance migrants and brightly colored birds are most affected
Biodiversity depressed by more than 50%
Micro Sv / hr .
25. Abundance of bumblebees and radiation
Moller & Mousseau. 2009. Biology Letters of the Royal Society
Micro Sv / hr .
26. Abundance of butterflies and radiation
Moller & Mousseau. 2009. Biology Letters of the Royal Society
Micro Sv / hr .
27. Abundance of spiders and radiation
Moller & Mousseau. 2009. Biology Letters of the Royal Society
Micro Sv / hr .
28. Moller and Mousseau. 2010. Ecological Indicators.
Mousseau and Moller. 2011. Bulletin of the Atomic Scientists.
29. Moller and Mousseau. 2010. Ecological Indicators.
Mousseau and Moller. 2011. Bulletin of the Atomic Scientists.
32. Mammals show significant declines in areas of high contamination.
Moller and Mousseau. 2010. Ecological Indicators.
Mousseau and Moller. 2011. Bulletin of the Atomic Scientists.
F=18.5, p<0.0001
36. Fukushima 2011 Chernobyl 2006-09
A.P. Møller, A. Hagiwara, S. Kasahara, S. Matsui, I. Nishiumi, H. Suzuki, K. Ueda and T. A. Mousseau. 2012. Environmental Pollution.
39. Major Findings from studies of Wildlife in Chernobyl and Fukushima:
1) Most organisms studied show significantly increased rates of genetic
damage in proportion to the level of exposure to radioactive
contaminants
2) Many organisms show increased rates of deformities and developmental
abnormalities in direct proportion to contamination levels
3) Many organisms show reduced fertility rates…..
4) Many organisms show reduced life spans……
5) Many organisms show reduced population sizes…..
1) Biodiversity is significantly decreased…… many species locally extinct.
40. The UN Chernobyl Forum Report
(IAEA, 2006: p137):
“. . . the populations of many plants and animals have
expanded, and the present environmental conditions have
had a positive impact on the biota in the Chernobyl
Exclusion Zone.”
New Results:
The question of whether or not abundances of some species (e.g. those subject to
hunting) are higher inside the zone is moot. There is now very strong evidence that
population abundances and biodiversity are negatively impacted in proportion to
level of radioactive contamination levels.
41.
42.
43. What are the developmental effects of
radiation-induced mutations?
Godzilla
44. Partially albinistic male swallow (on left). Swallows from Chernobyl region are
generally much paler than swallows from other regions.
Moller & Mousseau. 2001. Evolution
60. Moller, Mousseau, et al. 2011. PLoS One
Smaller brained
birds die younger
and appear to
have lower
“IQs”.
61. Selection against small heads
3.35
3.40
3.45
Yearling Older
Headvolume(cc)
Age
F = 9.92, df = 1,284, P = 0.0018
(Møller et al., PLoS One 6(2):e16862, 2011)
66. 0
20
40
60
Abnormalsperm(%)
0.01 0.1 1 10
Radiation (mR/h)
(a)
Moller, Mousseau & Surai. 2005. Proc. Roy. Soc. Lond. B.
Frequency of abnormal sperm is directly related to background radiation levels.